Transfection of pseudouridine-modified mRNA encoding CPD-photolyase leads to repair of DNA damage in human keratinocytes: A new approach with future therapeutic potential

Journal of Photochemistry and Photobiology B: Biology

Volumn 129, Issue , 2013, Pages 93-99

  Boros, Gábor ^a   Miko, Edit ^a   Muramatsu, Hiromi ^b   Weissman, Drew ^b   Emri, Eszter ^a   Rózsa, Dávid ^a   Nagy, Georgina ^a   Juhász, Attila ^a   Juhász, István ^a,c   Van Der Horst, Gijsbertus ^d   Horkay, Irén ^a   Remenyik, Éva ^a   Karikó, Katalin ^b   Emri, Gabriella ^a  

^a UNIVERSITY OF DEBRECEN   (Hungary)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF DEBRECEN   (Hungary)

^d ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Cyclobutane pyrimidine dimers; Human keratinocyte; mRNA therapy; Photolyase; Pseudouridine modified mRNA; UVB

Indexed keywords

DEOXYRIBODIPYRIMIDINE PHOTOLYASE; INTERLEUKIN 6; LIPOFECTAMINE; MESSENGER RNA; PSEUDOURIDINE; PYRIMIDINE DIMER;

ARTICLE; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; CUTANEOUS PARAMETERS; DNA REPAIR; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE MICROSCOPY; GENE THERAPY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; KERATINOCYTE; MARSUPIAL; MELANOGENESIS; NONHUMAN; PHOTOREACTIVATION; POTOROUS TRIDACTYLUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RNA TRANSCRIPTION; TRANSIENT EXPRESSION; TRANSIENT TRANSFECTION; ULTRAVIOLET B RADIATION;

METATHERIA; POTOROUS TRIDACTYLUS;

CYCLOBUTANE PYRIMIDINE DIMERS; HUMAN KERATINOCYTE; MRNA THERAPY; PHOTOLYASE; PSEUDOURIDINE-MODIFIED MRNA; UVB;

ANIMALS; CELL LINE; CELL PROLIFERATION; DEOXYRIBODIPYRIMIDINE PHOTO-LYASE; DNA REPAIR; HUMANS; INTERLEUKIN-6; KERATINOCYTES; LIGHT; LIPIDS; POTOROIDAE; PSEUDOURIDINE; PYRIMIDINE DIMERS; RNA, MESSENGER; TRANSFECTION; ULTRAVIOLET RAYS;

EID: 84887087798     PISSN: 10111344     EISSN: 18732682     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2013.09.010     Document Type: Article

References (61)

1. Y. Matsumura, and H.N. Ananthaswamy Toxic effects of ultraviolet radiation on the skin Toxicol. Appl. Pharmacol. 195 2004 298 308 (Pubitemid 38338650)
2. J. Cadet, C. Anselmino, T. Douki, and L. Voituriez Photochemistry of nucleic acids in cells J. Photochem. Photobiol., B 15 1992 277 298
3. M. Protic-Sabljic, N. Tuteja, P.J. Munson, J. Hauser, K.H. Kraemer, and K. Dixon UV light-induced cyclobutane pyrimidine dimers are mutagenic in mammalian cells Mol. Cell. Biol. 6 1986 3349 3356
4. E. Sage Distribution and repair of photolesions in DNA: genetic consequences and the role of sequence context Photochem. Photobiol. 57 1993 163 174
5. Y.H. You, D.H. Lee, J.H. Yoon, S. Nakajima, A. Yasui, and G.P. Pfeifer Cyclobutane pyrimidine dimers are responsible for the vast majority of mutations induced by UVB irradiation in mammalian cells J. Biol. Chem. 276 2001 44688 44694
6. G. Emri, E. Wenczl, P. Van Erp, J. Jans, L. Roza, I. Horkay, and A.A. Schothorst Low doses of UVB or UVA induce chromosomal aberrations in cultured human skin cells J Invest Dermatol 115 2000 435 440
7. J. de Boer, and J.H. Hoeijmakers Nucleotide excision repair and human syndromes Carcinogenesis 21 2000 453 460 (Pubitemid 30137930)
8. J.H. Hoeijmakers Nucleotide excision repair. II: from yeast to mammals Trends Genet. 9 1993 211 217 (Pubitemid 23165342)
9. T. Nouspikel DNA repair in mammalian cells: nucleotide excision repair: variations on versatility Cell. Mol. Life Sci. 66 2009 994 1009
10. A. Sancar DNA excision repair Annu. Rev. Biochem. 65 1996 43 81 (Pubitemid 26250604)
11. J.H. Hoeijmakers Genome maintenance mechanisms for preventing cancer Nature 411 2001 366 374 (Pubitemid 32467046)
12. L.H. Mullenders, A.M. Hazekamp-van Dokkum, W.H. Kalle, H. Vrieling, M.Z. Zdzienicka, and A.A. van Zeeland UV-induced photo lesions, their repair and mutations Mutat. Res. 299 1993 271 276 (Pubitemid 23115165)
13. R.P. Sinha, and D.P. Hader UV-induced DNA damage and repair: a review Photochem. Photobiol. Sci. 1 2002 225 236 (Pubitemid 37069733)
14. J.E. Hearst The structure of photolyase: using photon energy for DNA repair Science 268 1995 1858 1859
15. T. Carell, L.T. Burgdorf, L.M. Kundu, and M. Cichon The mechanism of action of DNA photolyases Curr. Opin. Chem. Biol. 5 2001 491 498 (Pubitemid 32907599)
16. Y.F. Li, S.T. Kim, and A. Sancar Evidence for lack of DNA photoreactivating enzyme in humans Proc. Natl. Acad. Sci. USA 90 1993 4389 4393 (Pubitemid 23148909)
17. S. Kanai, R. Kikuno, H. Toh, H. Ryo, and T. Todo Molecular evolution of the photolyase-blue-light photoreceptor family J. Mol. Evol. 45 1997 535 548 (Pubitemid 27461028)
18. C.F. Menck Shining a light on photolyases Nat. Genet. 32 2002 338 339 (Pubitemid 35266103)
19. A.P. Eker, C. Quayle, I. Chaves, and G.T. van der Horst DNA repair in mammalian cells: direct DNA damage reversal: elegant solutions for nasty problems Cell. Mol. Life Sci. 66 2009 968 980
20. H. Stege, L. Roza, A.A. Vink, M. Grewe, T. Ruzicka, S. Grether-Beck, and J. Krutmann Enzyme plus light therapy to repair DNA damage in ultraviolet-B-irradiated human skin Proc. Natl. Acad. Sci. USA 97 2000 1790 1795 (Pubitemid 30118521)
21. L. Roza, W. Vermeulen, J.B. Bergen Henegouwen, A.P. Eker, N.G. Jaspers, P.H. Lohman, and J.H. Hoeijmakers Effects of microinjected photoreactivating enzyme on thymine dimer removal and DNA repair synthesis in normal human and xeroderma pigmentosum fibroblasts Cancer Res. 50 1990 1905 1910 (Pubitemid 20098842)
22. J. Jans, W. Schul, Y.G. Sert, Y. Rijksen, H. Rebel, A.P. Eker, S. Nakajima, H. van Steeg, F.R. de Gruijl, A. Yasui, J.H. Hoeijmakers, and G.T. van der Horst Powerful skin cancer protection by a CPD-photolyase transgene Curr. Biol. 15 2005 105 115
23. K.K. Dong, N. Damaghi, S.D. Picart, N.G. Markova, K. Obayashi, Y. Okano, H. Masaki, S. Grether-Beck, J. Krutmann, K.A. Smiles, and D.B. Yarosh UV-induced DNA damage initiates release of MMP-1 in human skin Exp. Dermatol. 17 2008 1037 1044
24. A.A. Vink, A.M. Moodycliffe, V. Shreedhar, S.E. Ullrich, L. Roza, D.B. Yarosh, and M.L. Kripke The inhibition of antigen-presenting activity of dendritic cells resulting from UV irradiation of murine skin is restored by in vitro photorepair of cyclobutane pyrimidine dimers Proc. Natl. Acad. Sci. USA 94 1997 5255 5260
25. H. Stege Effect of xenogenic repair enzymes on photoimmunology and photocarcinogenesis J. Photochem. Photobiol., B 65 2001 105 108 (Pubitemid 34110724)
26. E. Berardesca, M. Bertona, K. Altabas, V. Altabas, and E. Emanuele Reduced ultraviolet-induced DNA damage and apoptosis in human skin with topical application of a photolyase-containing DNA repair enzyme cream: clues to skin cancer prevention Mol. Med. Report 5 2012 570 574
27. W. Schul, J. Jans, Y.M. Rijksen, K.H. Klemann, A.P. Eker, J. de Wit, O. Nikaido, S. Nakajima, A. Yasui, J.H. Hoeijmakers, and G.T. van der Horst Enhanced repair of cyclobutane pyrimidine dimers and improved UV resistance in photolyase transgenic mice EMBO J. 21 2002 4719 4729 (Pubitemid 34984359)
28. G.A. Garinis, J.R. Mitchell, M.J. Moorhouse, K. Hanada, H. de Waard, D. Vandeputte, J. Jans, K. Brand, M. Smid, P.J. van der Spek, J.H. Hoeijmakers, R. Kanaar, and G.T. van der Horst Transcriptome analysis reveals cyclobutane pyrimidine dimers as a major source of UV-induced DNA breaks EMBO J. 24 2005 3952 3962 (Pubitemid 41638001)
29. J. Jans, G.A. Garinis, W. Schul, A. van Oudenaren, M. Moorhouse, M. Smid, Y.G. Sert, A. van der Velde, Y. Rijksen, F.R. de Gruijl, P.J. van der Spek, A. Yasui, J.H. Hoeijmakers, P.J. Leenen, and G.T. van der Horst Differential role of basal keratinocytes in UV-induced immunosuppression and skin cancer Mol. Cell. Biol. 26 2006 8515 8526 (Pubitemid 44748584)
30. H. Asahina, Z. Han, M. Kawanishi, T. Kato Jr., H. Ayaki, T. Todo, T. Yagi, H. Takebe, M. Ikenaga, and S.H. Kimura Expression of a mammalian DNA photolyase confers light-dependent repair activity and reduces mutations of UV-irradiated shuttle vectors in xeroderma pigmentosum cells Mutat. Res. 435 1999 255 262
31. V. Chigancas, E.N. Miyaji, A.R. Muotri, J. de Fatima Jacysyn, G.P. Amarante-Mendes, A. Yasui, and C.F. Menck Photorepair prevents ultraviolet-induced apoptosis in human cells expressing the marsupial photolyase gene Cancer Res. 60 2000 2458 2463 (Pubitemid 30262437)
32. S. Nakajima, L. Lan, S. Kanno, M. Takao, K. Yamamoto, A.P. Eker, and A. Yasui UV light-induced DNA damage and tolerance for the survival of nucleotide excision repair-deficient human cells J. Biol. Chem. 279 2004 46674 46677 (Pubitemid 39518314)
33. M. Hamdi, J. Kool, P. Cornelissen-Steijger, F. Carlotti, H.E. Popeijus, C. van der Burgt, J.M. Janssen, A. Yasui, R.C. Hoeben, C. Terleth, L.H. Mullenders, and H. van Dam DNA damage in transcribed genes induces apoptosis via the JNK pathway and the JNK-phosphatase MKP-1 Oncogene 24 2005 7135 7144 (Pubitemid 41679276)
34. V. Chigancas, A. Sarasin, and C.F. Menck CPD-photolyase adenovirus-mediated gene transfer in normal and DNA-repair-deficient human cells J. Cell Sci. 117 2004 3579 3592 (Pubitemid 39206398)
35. K.M. de Lima-Bessa, M.G. Armelini, V. Chigancas, J.F. Jacysyn, G.P. Amarante-Mendes, A. Sarasin, and C.F. Menck CPDs and 6-4PPs play different roles in UV-induced cell death in normal and NER-deficient human cells DNA Repair (Amst) 7 2008 303 312
36. J.W. Schott, M. Galla, T. Godinho, C. Baum, and A. Schambach Viral and non-viral approaches for transient delivery of mRNA and proteins Curr. Gene Ther. 11 2011 382 398
37. A.N. Kuhn, T. Beibetaert, P. Simon, B. Vallazza, J. Buck, B.P. Davies, O. Tureci, and U. Sahin MRNA as a versatile tool for exogenous protein expression Curr. Gene Ther. 12 2012 347 361
38. G. Tavernier, O. Andries, J. Demeester, N.N. Sanders, S.C. De Smedt, and J. Rejman MRNA as gene therapeutic: how to control protein expression J Control Release 150 2011 238 247
39. K. Karikó, M. Buckstein, H. Ni, and D. Weissman Suppression of RNA recognition by toll-like receptors: the impact of nucleoside modification and the evolutionary origin of RNA Immunity 23 2005 165 175 (Pubitemid 41169286)
40. V. Hornung, J. Ellegast, S. Kim, K. Brzozka, A. Jung, H. Kato, H. Poeck, S. Akira, K.K. Conzelmann, M. Schlee, S. Endres, and G. Hartmann 5′-Triphosphate RNA is the ligand for RIG-I Science 314 2006 994 997
41. S.R. Nallagatla, and P.C. Bevilacqua Nucleoside modifications modulate activation of the protein kinase PKR in an RNA structure-specific manner RNA 14 2008 1201 1213 (Pubitemid 351717499)
42. K. Kariko, H. Muramatsu, F.A. Welsh, J. Ludwig, H. Kato, S. Akira, and D. Weissman Incorporation of pseudouridine into mRNA yields superior nonimmunogenic vector with increased translational capacity and biological stability Mol. Ther. 16 2008 1833 1840
43. B.R. Anderson, H. Muramatsu, B.K. Jha, R.H. Silverman, D. Weissman, and K. Kariko Nucleoside modifications in RNA limit activation of 2′-5′-oligoadenylate synthetase and increase resistance to cleavage by RNase L Nucleic Acids Res. 39 2011 9329 9338
44. B.R. Anderson, H. Muramatsu, S.R. Nallagatla, P.C. Bevilacqua, L.H. Sansing, D. Weissman, and K. Kariko Incorporation of pseudouridine into mRNA enhances translation by diminishing PKR activation Nucleic Acids Res. 38 2010 5884 5892
45. K. Kariko, H. Muramatsu, J. Ludwig, and D. Weissman Generating the optimal mRNA for therapy: HPLC purification eliminates immune activation and improves translation of nucleoside-modified, protein-encoding mRNA Nucleic Acids Res. 39 2011 e142
46. K. Kariko, H. Muramatsu, J.M. Keller, and D. Weissman Increased erythropoiesis in mice injected with submicrogram quantities of pseudouridine-containing mRNA encoding erythropoietin Mol. Ther. 20 2012 948 953
47. A. Balogh, G. Paragh Jr., A. Juhasz, T. Kobling, D. Torocsik, E. Miko, V. Varga, G. Emri, I. Horkay, B. Scholtz, and E. Remenyik Reference genes for quantitative real time PCR in UVB irradiated keratinocytes J. Photochem. Photobiol., B 93 2008 133 139
48. C. Petit-Frere, P.H. Clingen, M. Grewe, J. Krutmann, L. Roza, C.F. Arlett, and M.H. Green Induction of interleukin-6 production by ultraviolet radiation in normal human epidermal keratinocytes and in a human keratinocyte cell line is mediated by DNA damage J. Invest. Dermatol. 111 1998 354 359 (Pubitemid 28400076)
49. M. Grewe, H. Stege, A. Vink, M. Klammer, T. Ruzicka, L. Roza, and J. Krutmann Inhibition of intercellular adhesio nmolecule-1 (ICAM-1) expression in ultraviolet B-irradiated human antigen-presenting cells is restored after repair of cyclobutane pyrimidine dimers Exp. Dermatol. 9 2000 423 430
50. L. Decome, M. De Meo, A. Geffard, O. Doucet, G. Dumenil, and A. Botta Evaluation of photolyase (Photosome) repair activity in human keratinocytes after a single dose of ultraviolet B irradiation using the comet assay J. Photochem. Photobiol., B 79 2005 101 108 (Pubitemid 40614102)
51. A. Hofer, F.J. Legat, A. Gruber-Wackernagel, F. Quehenberger, and P. Wolf Topical liposomal DNA-repair enzymes in polymorphic light eruption Photochem. Photobiol. Sci. 10 2011 1118 1128
52. M. Nishinaga, R. Kurata, K. Onishi, K. Kuriyama, M. Wakasugi, and T. Matsunaga Establishment of a microplate-formatted cell-based immunoassay for rapid analysis of nucleotide excision repair ability in human primary cells Photochem. Photobiol. 88 2012 356 362
53. T.M. Runger, B. Farahvash, Z. Hatvani, and A. Rees Comparison of DNA damage responses following equimutagenic doses of UVA and UVB: a less effective cell cycle arrest with UVA may render UVA-induced pyrimidine dimers more mutagenic than UVB-induced ones Photochem. Photobiol. Sci. 11 2012 207 215
54. C. Robert, B. Muel, A. Benoit, L. Dubertret, A. Sarasin, and A. Stary Cell survival and shuttle vector mutagenesis induced by ultraviolet A and ultraviolet B radiation in a human cell line J. Invest. Dermatol. 106 1996 721 728 (Pubitemid 26119730)
55. V. Chigancas, L.F. Batista, G. Brumatti, G.P. Amarante-Mendes, A. Yasui, and C.F. Menck Photorepair of RNA polymerase arrest and apoptosis after ultraviolet irradiation in normal and XPB deficient rodent cells Cell Death Differ. 9 2002 1099 1107
56. A. Schwarz, R. Bhardwaj, Y. Aragane, K. Mahnke, H. Riemann, D. Metze, T.A. Luger, and T. Schwarz Ultraviolet-B-induced apoptosis of keratinocytes: evidence for partial involvement of tumor necrosis factor-alpha in the formation of sunburn cells J. Invest. Dermatol. 104 1995 922 927
57. L. Marrot, and J.R. Meunier Skin DNA photodamage and its biological consequences J. Am. Acad. Dermatol. 58 2008 S139 S148
58. C.D. Enk, M. Hochberg, A. Torres, O. Lev, I. Dor, M. Srebnik, and V.M. Dembitsky Photoprotection by Cichorum endivia extracts: prevention of UVB-induced erythema, pyrimidine dimer formation and IL-6 expression Skin Pharmacol. Physiol. 17 2004 42 48 (Pubitemid 38250479)
59. J. Narbutt, A. Lesiak, A. Sysa-Jedrzejowska, A. Wozniacka, A. Cierniewska-Cieslak, J. Boncela, C. Jochymski, W. Kozlowski, A. Zalewska, M. Skibinska, and M. Norval Repeated low-dose ultraviolet (UV) B exposures of humans induce limited photoprotection against the immune effects of erythemal UVB radiation Br. J. Dermatol. 156 2007 539 547
60. J.J. Bernard, C. Cowing-Zitron, T. Nakatsuji, B. Muehleisen, J. Muto, A.W. Borkowski, L. Martinez, E.L. Greidinger, B.D. Yu, R.L. Gallo, Ultraviolet radiation damages self noncoding RNA and is detected by TLR3, Nat Med (2012).
61. B.A. Gilchrest, and M.S. Eller DNA photodamage stimulates melanogenesis and other photoprotective responses J. Investig. Dermatol. Sympos. Proc. 4 1999 35 40 (Pubitemid 29491252)